Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-17T12:23:24.574Z Has data issue: false hasContentIssue false

Genotyping of Theileria parva populations in vaccinated and non-vaccinated cattle in Malawi

Published online by Cambridge University Press:  11 April 2022

Elisha Chatanga
Affiliation:
Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Kita-18, Nishi-9, Sapporo, Hokkaido 060-0818, Japan Department of Veterinary Pathobiology, Lilongwe University of Agriculture and Natural Resources, P.O. Box 219, Lilongwe, Malawi
Yuma Ohari
Affiliation:
Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Kita-18, Nishi-9, Sapporo, Hokkaido 060-0818, Japan
Walter Muleya
Affiliation:
Department of Biomedical Sciences, School of Veterinary Medicine, University of Zambia, P.O. Box 32379, Lusaka, Zambia
Kyoko Hayashida
Affiliation:
Division of Collaboration and Education, International Institute for Zoonosis Control, Hokkaido University, Kita-20, Nishi-10, Sapporo, Hokkaido 001-0020, Japan
Chihiro Sugimoto
Affiliation:
Division of Collaboration and Education, International Institute for Zoonosis Control, Hokkaido University, Kita-20, Nishi-10, Sapporo, Hokkaido 001-0020, Japan
Ken Katakura
Affiliation:
Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Kita-18, Nishi-9, Sapporo, Hokkaido 060-0818, Japan
Nariaki Nonaka
Affiliation:
Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Kita-18, Nishi-9, Sapporo, Hokkaido 060-0818, Japan
Ryo Nakao*
Affiliation:
Laboratory of Parasitology, Graduate School of Infectious Diseases, Faculty of Veterinary Medicine, Hokkaido University, Kita-18, Nishi-9, Sapporo, Hokkaido 060-0818, Japan
*
Author for correspondence: Ryo Nakao, E-mail: [email protected]

Abstract

Theileria parva is an apicomplexan protozoan parasite that causes bovine theileriosis (East Coast Fever; ECF) in central, eastern and southern Africa. In Malawi, ECF is endemic in the northern and central regions where it has negatively affected the development of dairy industry. Despite its endemic status the genetic population structure of T. parva in Malawi is currently unknown. To obtain an understanding of T. parva in Malawi, we performed population genetics analysis of T. parva populations in cattle vaccinated with the Muguga cocktail live vaccine and non-vaccinated cattle using mini- and microsatellite markers covering all the four T. parva chromosomes. The T. parva Muguga strain was included in this study as a reference strain. Linkage disequilibrium was observed when all samples were treated as a single population. There was sub-structuring among the samples as shown by the principal coordinate analysis. Majority of the samples clustered with the T. parva Muguga reference strain suggesting that the isolates in Malawi are closely related to the vaccine component, which support the current use of Muguga cocktail vaccine to control ECF. The clustering of samples from non-endemic southern region with those from endemic central region suggests expansion of the distribution of T. parva in Malawi.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Atuhaire, DK, Muleya, W, Mbao, V, Niyongabo, J, Nyabongo, L, Nsanganiyumwami, D, Salt, J, Namangala, B and Musoke, AJ (2021) Molecular characterization and population genetics of Theileria parva in Burundi's unvaccinated cattle: towards the introduction of East Coast fever vaccine. PLoS ONE 16, e0251500.CrossRefGoogle ScholarPubMed
Bowcock, AM, Ruiz-Linares, A, Tomfohrde, J, Minch, E, Kidd, JR and Cavalli-Sforza, LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368, 455457.CrossRefGoogle ScholarPubMed
Chatanga, E, Hayashida, K, Muleya, W, Kusakisako, K, Moustafa, MAM, Salim, B, Katakura, K, Sugimoto, C, Nonaka, N and Nakao, R (2020) Genetic diversity and sequence polymorphism of two genes encoding Theileria parva antigens recognized by CD8+ T cells among vaccinated and unvaccinated cattle in Malawi. Pathogens (Basel, Switzerland) 9, 334.Google ScholarPubMed
Chinombo, DO, Mzoma, FJ and Musisi, FL (1988). East Coast Fever in Malawi (1983–1987). Theileriosis in Eastern, Central and Southern Africa. In Proceedings of a Workshop on East Coast Fever Immunization, Lilongwe, Malawi, 20–22 September 1988, Dolan, T.T, Ed, ILRAD: Nairobi, Kenya, pp. 12–16.Google Scholar
DAHLD (2006) Policy Document on Livestock in Malawi. Reducing Poverty Through Sustainable, Private Sector/Farmer Driven Livestock Production in Malawi. Lilongwe, Malawi: Department of Animal Health and Livestock Development. Ministry of Agriculture.Google Scholar
Dolan, TT (ed.) (1988) Theileriosis in Eastern, Central and Southern Africa. In Proceedings of a Workshop on East Coast Fever Immunization, Lilongwe, Malawi, 20–22 September 1988; Nairobi, Kenya: ILRAD.Google Scholar
Gardner, MJ, Bishop, R, Shah, T, De Villiers, EP, Carlton, JM, Hall, N, Ren, Q, Paulsen, IT, Pain, A, Berriman, M, Wilson, RJM, Sato, S, Ralph, SA, Mann, DJ, Xiong, Z, Shallom, SJ, Weidman, J, Jiang, L, Lynn, J, Weaver, B, Shoaibi, A, Domingo, AR, Wasawo, D, Crabtree, J, Wortman, JR, Haas, B, Angiuoli, SV, Creasy, TH, Lu, C, Suh, B, Silva, JC, Utterback, TR, Feldblyum, TV, Pertea, M, Allen, J, Nierman, WC, Taracha, ELN, Salzberg, SL, White, OR, Fitzhugh, HA, Morzaria, S, Venter, JC, Fraser, CM and Nene, V (2005) Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science (New York, N.Y.) 309, 134137.CrossRefGoogle ScholarPubMed
Haubold, B and Hudson, RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage analysis. Bioinformatics (Oxford, England) 16, 847848.CrossRefGoogle ScholarPubMed
Katzer, F, Daniel, N, Chris, O, Bishop, RP, Evans, LN, Taracha, ARW and Declan, JM (2006) Extensive genotypic diversity in a recombining population of the apicomplexan parasite Theileria parva. Infection and Immunity 74, 54565464.CrossRefGoogle Scholar
Katzer, F, Ngugi, D, Walker, AR and McKeever, DJ (2010) Genotypic diversity, a survival strategy for the apicomplexan parasite Theileria parva. Veterinary Parasitology 167, 236243.CrossRefGoogle ScholarPubMed
Lawrence, JA, Musisi, FL, Mfitilodze, MW, Tjornehoj, K, Whiteland, AP, Kafuwa, PT and Chamambala, KE (1996) Integrated tick and tick-borne disease control trials in crossbred dairy cattle in Malawi. Tropical Animal Health and Production 28, 280288.CrossRefGoogle ScholarPubMed
Lubembe, DM, Odongo, DO, Salih, DA and Sibeko-Matjila, KP (2020) Microsatellite and minisatellite genotyping of Theileria parva population from southern Africa reveals possible discriminatory allele profiles with parasites from eastern Africa. Ticks and Tick-Borne Diseases 11, 101539.CrossRefGoogle ScholarPubMed
Marcellino, WL, Salih, DA, Njahira, MN, Ndiwa, N, Araba, A, El Hussein, AM, Seitzer, U, Ahmed, JS, Bishop, RP and Skilton, RA (2017) The emergence of Theileria parva in Jonglei state, South Sudan: confirmation using molecular and serological diagnostic tools. Transboundary Emerging Diseases 64, 12291235.CrossRefGoogle ScholarPubMed
Moll, G, Lohding, A and Young, A (1984) Epidemiology of theilerioses in the Trans-Mara division Kenya: husbandry and disease background and preliminary investigations on theilerioses in calves. Preventive Veterinary Medicine 2, 801831.CrossRefGoogle Scholar
Moll, G, Lohding, A, Young, A and Leitch, B (1986) Epidemiology of theileriosis in calves in an endemic area of Kenya. Veterinary Parasitology 19, 255273.CrossRefGoogle Scholar
Muleya, W, Namangala, B, Simuunza, M, Nakao, R, Inoue, N, Kimura, T, Ito, K, Sugimoto, C and Sawa, H (2012) Population genetic analysis and sub-structuring of Theileria parva in the northern and eastern parts of Zambia. Parasites & Vectors 5, 255.CrossRefGoogle ScholarPubMed
Odongo, D, Sunter, JD, Kiara, HK, Skilton, RA and Bishop, RP (2010) A nested PCR assay exhibits enhanced sensitivity for detection of Theileria parva infections in bovine blood samples from carrier animals. Parasitology Research 106, 357365.CrossRefGoogle ScholarPubMed
Oura, CA, Odongo, DO, Lubega, GW, Spooner, PR, Tait, A and Bishop, RP (2003) A panel of microsatellite and minisatellite markers for the characterisation of field isolates of Theileria parva. International Journal for Parasitology 33, 16411653.CrossRefGoogle ScholarPubMed
Oura, CA, Asiimwe, BB, Weir, W, Lubega, GW and Tait, A (2005) Population genetic analysis and sub-structuring of Theileria parva in Uganda. Molecular and Biochemical Parasitology 140, 229239.CrossRefGoogle ScholarPubMed
Oura, CAL, Bishop, R, Asiimwe, BB, Spooner, P, Lubega, GW and Tait, A (2007) Theileria parva live vaccination: parasite transmission, persistence and heterologous challenge in the field. Parasitology 134, 12051213.CrossRefGoogle ScholarPubMed
Peakall, R and Smouse, PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Molecular and Ecology Notes 6, 288295.CrossRefGoogle Scholar
Peakall, R and Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics (Oxford, England) 28, 25372539.CrossRefGoogle ScholarPubMed
Perry, B (2016) The control of East Coast fever of cattle by live parasite vaccination: a science-to-impact narrative. One Health (Amsterdam, Netherlands) 2, 103114.Google ScholarPubMed
Rukambile, E, Machuka, E, Njahira, M, Kyalo, M, Skilton, R, Mwega, E, Chota, A, Mathias, M, Sallu, R and Salih, D (2016) Population genetic analysis of Theileria parva isolated in cattle and buffaloes in Tanzania using minisatellite and microsatellite markers. Veterinary Parasitology 224, 2026.CrossRefGoogle ScholarPubMed
Salih, DA, Mwacharo, JM, Pelle, R, Njahira, MN, Odongo, DO, Mbole-Kariuki, MN, Marcellino, WL, Malak, AK, Kiara, H, El Hussein, ARM, Bishop, RP and Skilton, RA (2018) Genetic diversity and population structure of Theileria parva in South Sudan. Ticks and Tick-Borne Diseases 9, 806813.CrossRefGoogle ScholarPubMed